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Tannin sensitivity in larvae ofMalacosoma disstria (Lepidoptera): Roles of the peritrophic envelope and midgut oxidation

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Abstract

Final-instarMalacosoma disstria fed artificial diets containing tannic acid develop lethal pupal deformities. We examined some of the factors potentially underlying tannin sensitivity in this species, including the permeability of the peritrophic envelope to tannic acid and the chemical fate of tannic acid in the gut. Tannic acid does not penetrate the peritrophic envelope ofM. disstria, demonstrating that the containment of tannic acid within the endoperitrophic space is not sufficient to protect an insect herbivore from the adverse effects of ingested tannins. Ingested tannic acid undergoes extensive chemical modification in the midgut. Only 19–21 % of the high molecular weight components of the tannic acid ingested was recovered in the frass. Of two possible chemical fates of ingested tannic acid, oxidation is the predominant chemical transformation, whereas little hydrolysis occurs. Measurements of gut redox parameters showed that conditions in the midgut favor the oxidation of phenols. However, similar conditions occur in the midguts ofOrgyia leucostigma, in which no oxidation occurs. Therefore, oxidizing gut redox conditions do not necessarily lead to polyphenol oxidation in lepidopteran larvae. We conclude that the sensitivity ofM. disstria to ingested tannins is a consequence of their oxidation in the midgut.

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References

  • Adang, M.J., andSpence, K.D. 1983. Permeability of the peritrophic membrane of the Douglas fir tussock moth (Orgyia pseudotsugata).Comp. Biochem. Physiol. 75A:233–238.

    Google Scholar 

  • Addy, N.D. 1969. Rearing the forest tent caterpillar on an artificial diet.J. Econ. Entomol. 62:270–271.

    Google Scholar 

  • Appel, H.M. 1993. Phenolics in ecological interactions: the importance of oxidation.J. Chem. Ecol. 19:1521–1552.

    Google Scholar 

  • Appel, H.M., andMartin, M.M. 1990. Gut redox conditions in herbivorous lepidopteran larvae.J. Chem. Ecol. 16:3277–3290.

    Google Scholar 

  • Austin, P.J., Suchar, L.A., Robbins, C.T., andHagerman, A.E. 1989. Tannin binding proteins in the saliva of deer and their absence in the saliva of sheep and cattle.J. Chem. Ecol. 15:1335–1347.

    Google Scholar 

  • Barbehenn, R.V., andMartin, M.M. 1992. The protective role of the peritrophic membrane in the tannin-tolerant larvae ofOrgyia leucostigma (Lepidoptera).J. Insect Physiol. 38:973–980.

    Google Scholar 

  • Berenbaum, M. 1983. Effect of tannins on growth and digestion in two species of papilionids.Entomol. Exp. Appl. 34:245–250.

    Google Scholar 

  • Bernays, E.A., Chamberlain, D., andMcCarthy, P. 1980. The differential effects of ingested tannic acid on different species of Acridoidea.Entomol. Exp. Appl. 28:158–166.

    Google Scholar 

  • Bernays, E.A., Chamberlain, D.J., andWoodhead, S. 1983. Phenols as nutrients for a phytophagous insectAnacridium melanorhodon.J. Insect Physiol. 29:535–539.

    Google Scholar 

  • Chang, R.L.S., Deen, W.M., Robertson, C.R., andBrenner, B.M. 1975. Permselectivity of the glomerular capillary wall: III. Restricted transport of polyanions.Kidney Int. 8:212–218.

    PubMed  Google Scholar 

  • Chippendale, G.M., Beck, S.D., andStrong, F.M. 1964. Methyl linolenate as an essential nutrient for the cabbage looper,Trichoplusia ni (Hübner).Nature 204:710–711.

    Google Scholar 

  • Cilliers, J.J.L., andSingleton, V.L. 1989. Nonenzymic autoxidative phenolic browning reactions in a caffeic acid model system.J. Agric. Food Chem. 37:390–396.

    Google Scholar 

  • Dadd, R.H. 1981. Essential fatty acids for mosquitoes, other insects and vertebrates, pp. 189–214,in G. Bhaskaran, S. Friedman, and J.G. Rodriguez (eds.). Current Topics in Insect Endocrinology and Nutrition. Plenum Press, New York.

    Google Scholar 

  • De Veau, E.J.I., andSchultz, J.C. (1992). Reassessment of the interaction between gut detergents and phenolics in Lepidoptera and significance for gypsy moth larvae.J. Chem. Ecol. 18:1437–1453.

    Google Scholar 

  • Dow, J.A.T. 1986 Insect midgut function.Adv. Insect Physiol. 19:188–328.

    Google Scholar 

  • Feeny, P. 1968. Effect of oak leaf tannins on larval growth of the winter mothOperophtera brumata.J. Insect Physiol. 14:805–817.

    Google Scholar 

  • Feeny, P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology 51:565–581.

    Google Scholar 

  • Feeny, P. 1976. Plant apparency and chemical defense, pp. 1–40,in J.W. Wallace and R.L. Mansell (eds.). Biochemical Interactions Between Plants and Insects. Plenum Press, New York.

    Google Scholar 

  • Felton, G.W., andDuffey, S.S. 1991. Protective action of midgut catalase in lepidopteran larvae against oxidative plant defenses.J. Chem. Ecol. 17:1715–1732.

    Google Scholar 

  • Felton, G.W., andDuffey, S.S. 1992. Ascorbate oxidation reduction inHelicoverpa zea as a scavenging system against dietary oxidants.Arch. Insect Biochem. Physiol. 19:27–37.

    Google Scholar 

  • Felton, G.W., Donato, K., Del Vecchio, R.J., andDuffey, S.S. 1989. Activation of plant polyphenol oxidases by insect feeding reduces the nutritive quality of foliage for noctuid herbivores.J. Chem. Ecol. 15:2667–2694.

    Google Scholar 

  • Hagerman, A.E. 1989. Chemistry of tannin-protein complexation, pp. 323–333,in R.W. Hemingway and J.J. Karchesy (eds.). Chemistry and Significance of Condensed Tannins. Plenum Publishing Corp., New York.

    Google Scholar 

  • Hagerman, A.E., andButler, L.G. 1991. Tannins and lignins, pp. 355–388,in G.A. Rosenthal and M.R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, 2nd ed., Vol. 1: The Chemical Participants. Academic Press, San Diego, California.

    Google Scholar 

  • Hathway, D.E., andSeakins, J.W.T. 1957. Autoxidation of polyphenols. Part 3. Autoxidation in neutral aqueous solution of flavans related to catechin.J. Chem. Soc. 2:1562–1566.

    Google Scholar 

  • Igarashi, K., andYasui, T. 1985. Oxidation of free methionine and methionine residues in protein involved in the browning reaction of phenolic compounds.Agric. Biol. Chem. 49:2309–2315.

    Google Scholar 

  • Ikeda, I., Imasato, Y., Sasaki, E., Nakayama, M., Nagao, H., Takeo, T., Yayabe, F., andSugano, M. 1992. Tea catechins decrease micellar solubility and intestinal absorption of cholesterol in rats.Biochim. Biophys. Acta 1127:141–146.

    PubMed  Google Scholar 

  • Inoue, K.H., andHagerman, A.E. 1988. Determination of gallotannin with rhodanine.Anal. Biochem. 169:363–369.

    PubMed  Google Scholar 

  • Isman, M.B., andDuffey, S.S. 1982. Toxicity of tomato phenolic compounds to the fruitworm,Heliothis zea. Entomol. Exp. Appl. 31:370–376.

    Google Scholar 

  • Karowe, D. 1989. Differential effect of tannic acid on two tree-feeding Lepidoptera: Implications for theories of plant-herbivore chemistry.Oecologia 80:507–512.

    Google Scholar 

  • Kato, M. 1978. Phenols as indispensible components of the synthetic diet of the silkworm,Bombyx mori.Entomol. Exp. Appl. 24:284–290.

    Google Scholar 

  • Klocke, J.A., andChan, B.G. 1982. Effects of cotton condensed tannin on feeding and digestion in the cotton pest,Heliothis zea.J. Insect Physiol. 28:911–915.

    Google Scholar 

  • Larson, R.A. 1988. The antioxidants of higher plants.Phytochemistry 27:969–978.

    Google Scholar 

  • Lea, C.H. 1962. The oxidative deterioration of food lipids, pp. 3–28,in H.W. Schultz (ed.). Symposium in Foods: Lipids and their Oxidation. Avi Publishing, Westport, Connecticut.

    Google Scholar 

  • Leatham, G.F., King, V., andStahmann, M.A. 1980. In vitro protein polymerization by quinones or free radicals generated by plant or fungal oxidative enzymes.Phytopathology 70:1134–1140.

    Google Scholar 

  • Lindsay, W.L. 1979. Chemical Equilibria in Soils. John Wiley & Sons, New York.

    Google Scholar 

  • Manuwoto, S., andScriber, J.M. 1986. Effects of hydrolyzable and condensed tannin on growth and development of two species of polyphagous Lepidoptera:Spodoptera eridania andCallosamia promethea.Oecologia 69:225–230.

    Google Scholar 

  • Manuwoto, S., Scriber, J.M., Hsia, M.T., andSunarjo, P. 1985. Antibiosis/antixenosis in tulip tree and quaking aspen leaves against the polyphagous southern armyworm,Spodoptera eridania.Oecologia 67:1–7.

    Google Scholar 

  • Miller, N., andLehane, M.J. 1993. Ionic environment and the permeability properties of the peritrophic membrane ofGlossina morsitans morsitans.J. Insect Physiol. 39:139–144.

    Google Scholar 

  • Rehr, S.S., Janzen, D.H., andFeeny, P.P. 1973.l-Dopa in legume seeds: A chemical barrier to insect attack.Science 181:81–82.

    Google Scholar 

  • Rhoades, D.F., andCates, R.G. 1976. Toward a general theory of plant antiherbivore chemistry.Recent Adv. Phytochem. 10:168–213.

    Google Scholar 

  • Rosenthal, G.A. 1977. The biological effects and mode of action ofl-canavanine, a structural analogue ofl-arginine.Q. Rev. Biol. 52:155–178.

    PubMed  Google Scholar 

  • Santos, C.D., andTerra, W.R. 1986. Distribution and characterization of oligomeric digestive enzymes fromErinnyis ello larvae and inferences concerning secretory mechanisms and the permeability of the peritrophic membrane.Insect Biochem. 16:691–700.

    Google Scholar 

  • Schultz, J.C. 1989. Tannin-insect interactions, pp. 417–433,in R.W. Hemingway and J.J. Karchesy (eds.). Chemistry and Significance of Condensed Tannins. Plenum Press, New York.

    Google Scholar 

  • Stehr, F.W., andCook, E.F. 1968. A revision of the genusMalacosoma Hübner in North Americana (Lepidoptera: Lasiocampidae): Systematics, biology, immatures, and parasites. Smithsonian Institution Press, Washington, D.C.

    Google Scholar 

  • Steinly, B.A., andBerenbaum, M. 1985. Histopathological effects of tannins on the midgut epithelium ofPapilio polyxenes andPapilio glaucus.Entomol. Exp. Appl. 39:3–9.

    Google Scholar 

  • Summers, C.B., andFelton, F.W. 1993. Antioxidant role of dehydroascorbic acid reductase in insects.Biochim. Biophys. Acta 1156:235–238.

    PubMed  Google Scholar 

  • Thomson, R.H. 1962. Some naturally occurring black pigments, pp. 99–113,in T.S. Gore, B.S. Joshi, S.V. Sunthankar, and B.D. Tilak (eds.). Recent Progress in the Chemistry of Natural and Synthetic Colouring Matters and Related Fields. Academic Press, New York.

    Google Scholar 

  • Wolfersberger, M.G., Spaeth, D.D., andDow, J.A.T. 1986. Permeability of the peritrophic membrane of tobacco hornworm larval midgut.Am. Zool. 26:74A.

    Google Scholar 

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  1. Department of Biology, University of Michigan, 48109-1048, Ann Arbor, Michigan

    Raymond V. Barbehenn & Michael M. Martin

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  1. Raymond V. Barbehenn
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Barbehenn, R.V., Martin, M.M. Tannin sensitivity in larvae ofMalacosoma disstria (Lepidoptera): Roles of the peritrophic envelope and midgut oxidation. J Chem Ecol 20, 1985–2001 (1994). https://doi.org/10.1007/BF02066238

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